Formation of Polyomavirus-Like Particles with Different VP1 Molecules That Bind the Urokinase Plasminogen Activator Receptor

Journal of Virology

Volumn 77, Issue 21, 2003, Pages 11491-11498

  Shin, Young C ^a,b   Folk, William R ^a  

^a University of Missouri   (United States)

^b HARVARD MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CAPSID PROTEIN; CELL SURFACE RECEPTOR; EPITOPE; NANOPARTICLE; NUCLEIC ACID; PROTEIN; PROTEIN VP1; UROKINASE; UROKINASE RECEPTOR;

AMINO ACID SEQUENCE; AMINO TERMINAL SEQUENCE; ANIMAL CELL; ARTICLE; CELL SURFACE; CONTROLLED STUDY; DRUG DELIVERY SYSTEM; GENE DELIVERY SYSTEM; HUMAN; HUMAN CELL; INSECT CELL; NONHUMAN; PHAGE DISPLAY; POLYOMA VIRUS; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN STRUCTURE; PROTEIN TARGETING; SOLUBILITY; VIRUS PARTICLE;

ANIMALS; BACULOVIRIDAE; CAPSID PROTEINS; CELL LINE; CELLS, CULTURED; GUINEA PIGS; HEMAGGLUTINATION TESTS; HUMANS; INSECTS; PLASMINOGEN ACTIVATORS; POLYOMAVIRUS; RECEPTORS, CELL SURFACE; VIRION;

EID: 0142028883     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.77.21.11491-11498.2003     Document Type: Article

References (67)

1. An, K., E. T. Gillock, J. A. Sweat, W. M. Reeves, and R. A. Consigli. 1999. Use of the baculovirus system to assemble polyomavirus capsid-like particles with different polyomavirus structural proteins: analysis of the recombinant assembled capsid-like particles. J. Gen. Virol. 80:1009-1016.
2. Appella, E., E. A. Robinson, S. J. Ullrich, M. P. Stoppelli, A. Corti, G. Cassani, and F. Blasi. 1987. The receptor-binding sequence of urokinase. A biological function for the growth-factor module of proteases. J. Biol. Chem. 262:4437-4440.
3. Bauer, P. H., R. T. Bronson, S. C. Fung, R. Freund, T. Stehle, S. C. Harrison, and T. L. Benjamin. 1995. Genetic and structural analysis of a virulence determinant in polyomavirus VP1. J. Virol. 69:7925-7931.
4. Braun, H., K. Boller, J. Lower, W. M. Bertling, and A. Zimmer. 1999. Oligonucleotide and plasmid DNA packaging into polyoma VP1 virus-like particles expressed in Escherichia coli. Biotechnol. Appl. Biochem. 29:31-43.
5. Busso, N., S. K. Masur, D. Lazega, S. Waxman, and L. Ossowski. 1994. Induction of cell migration by pro-urokinase binding to its receptor: possible mechanism for signal transduction in human epithelial cells. J. Cell Biol. 126:259-270.
6. Caruso, M., L. Belloni, O. Sthandier, P. Amati, and M. I. Garcia. 2003. α4β1 integrin acts as a cell receptor for murine polyomavirus at the postattachment level. J. Virol. 77:3913-3921.
7. Chapman, H. A. 1997. Plasminogen activators, integrins, and the coordinated regulation of cell adhesion and migration. Curr. Opin. Cell Biol. 9:714-724.
8. Chen, M. H., and T. Benjamin. Roles of N-glycans with alpha2, 6 as well as alpha2, 3 linked sialic acid in infection by polyoma virus. Virology 233:440-442.
9. Chiaradonna, F., L. Fontana, C. Iavarone, M. V. Carriero, G. Scholz, M. V. Barone, and M. P. Stoppelli. 1999. Urokinase receptor-dependent and -independent p56/59(hck) activation state is a molecular switch between myelomonocytic cell motility and adherence. EMBO J. 18:3013-3023.
10. Crowley, C. W., R. L. Cohen, B. K. Lucas, G. Liu, M. A. Shuman, and A. D. Levinson. 1993. Prevention of metastasis by inhibition of the urokinase receptor. Proc. Natl. Acad. Sci. USA 90:5021-5025.
11. Czekay, R. P., T. A. Kuemmel, R. A. Orlando, and M. G. Farquhar. 2001. Direct binding of occupied urokinase receptor (uPAR) to LDL receptor-related protein is required for endocytosis of uPAR and regulation of cell surface urokinase activity. Mol. Biol. Cell 12:1467-1479.
12. Drapkin, P. T., C. R. O'Riordan, S. M. Yi, J. A. Chiorini, J. Cardella, J. Zabner, and M. J. Welsh. 2000. Targeting the urokinase plasminogen activator receptor enhances gene transfer to human airway epithelia. J. Clin. Investig. 105:589-596.
13. Estreicher, A., J. Muhlhauser, J. L. Carpentier, L. Orci, and J. D. Vassalli. 1990. The receptor for urokinase type plasminogen activator polarizes expression of the protease to the leading edge of migrating monocytes and promotes degradation of enzyme inhibitor complexes. J. Cell Biol. 111:783-792.
14. Fazioli, F., M. Resnati, N. Sidenius, Y. Higashimoto, E. Appella, and F. Blasi. 1997. A urokinase-sensitive region of the human urokinase receptor is responsible for its chemotactic activity. EMBO J. 16:7279-7286.
15. Fibbi, G., M. Ziche, L. Morbidelli, L. Magnelli, and M. Del Rosso. 1988. Interaction of urokinase with specific receptors stimulates mobilization of bovine adrenal capillary endothelial cells. Exp. Cell Res. 179:385-395.
16. Forstova, J., N. Krauzewicz, V. Sandig, J. Elliott, Z. Palkova, M. Strauss, and B. E. Griffin. 1995. Polyoma virus pseudocapsids as efficient carriers of heterologous DNA into mammalian cells. Hum. Gene Ther. 6:297-306.
17. Freund, R., A. Calderone, C. J. Dawe, and T. L. Benjamin. 1991. Polyomavirus tumor induction in mice: effects of polymorphisms of VP1 and large T antigen. J. Virol. 65:335-341.
18. Fried, H., L. D. Cahan, and J. C. Paulson. 1981. Polyoma virus recognizes specific sialyligosaccharide receptors on host cells. Virology 109:188-192.
19. Gilbert, J. M., and T. L. Benjamin. 2000. Early steps of polyomavirus entry into cells. J. Virol. 74:8582-8588.
20. Gillock, E. T., S. Rottinghaus, D. Chang, X. Cai, S. A. Smiley, K. An, and R. A. Consigli. 1997. Polyomavirus major capsid protein VP1 is capable of packaging cellular DNA when expressed in the baculovirus system. J. Virol. 71:2857-2865.
21. Gleiter, S., and H. Lilie. 2001. Coupling of antibodies via protein Z on modified polyoma virus-like particles. Protein Sci. 10:434-444.
22. Gleiter, S., K. Stubenrauch, and H. Lilie. 1999. Changing the surface of a virus shell fusion of an enzyme to polyoma VP1. Protein Sci. 8:2562-2569.
23. Gollan, T. J., and M. R. Green. 2002. Selective targeting and inducible destruction of human cancer cells by retroviruses with envelope proteins bearing short peptide ligands. J. Virol. 76:3564-3569.
24. Goodson, R. J., M. V. Doyle, S. E. Kaufman, and S. Rosenberg. 1994. High-affinity urokinase receptor antagonists identified with bacteriophage peptide display. Proc. Natl. Acad. Sci. USA 91:7129-7133.
25. Griffiths, J. C., S. J. Harris, G. T. Layton, E. L. Berrie, T. J. French, N. R. Burns, S. E. Adams, and A. J. Kingsman. 1993. Hybrid human immunodeficiency virus Gag particles as an antigen carrier system: induction of cytotoxic T-cell and humoral responses by a Gag:V3 fusion. J. Virol. 67:3191-3198.
26. Gross, T. J., R. H. Simon, and R. G. Sitrin. 1990. Expression of urokinase-type plasminogen activator by rat pulmonary alveolar epithelial cells. Am. J. Respir. Cell Mol. Biol. 3:449-456.
27. Gudewicz, P. W., and N. Gilboa. 1987. Human urokinase-type plasminogen activator stimulates chemotaxis of human neutrophils. Biochem. Biophys. Res. Commun. 147:1176-1181.
28. Gyetko, M. R., R. F. Todd III, C. C. Wilkinson, and R. G. Sitrin. 1994. The urokinase receptor is required for human monocyte chemotaxis in vitro. J. Clin. Investig. 93:1380-1387.
29. Hearing, V. J., L. W. Law, A. Corti, E. Appella, and F. Blasi. 1988. Modulation of metastatic potential by cell surface urokinase of murine melanoma cells. Cancer Res. 48:1270-1278.
30. Hollas, W., N. Hoosein, L. W. Chung, A. Mazar, J. Henkin, K. Kariko, E. S. Barnathan, and D. Boyd. 1992. Expression of urokinase and its receptor in invasive and non-invasive prostate cancer cell lines. Thromb. Haemost. 68:662-666.
31. Hoosein, N. M., D. D. Boyd, W. J. Hollas, A. Mazar, J. Henkin, and L. W. Chung. 1991. Involvement of urokinase and its receptor in the invasiveness of human prostatic carcinoma cell lines. Cancer Commun. 3:255-264.
32. Jankun, J., H. W. Merrick, and P. J. Goldblatt. 1993. Expression and localization of elements of the plasminogen activation system in benign breast disease and breast cancers. J. Cell. Biochem. 53:135-144.
33. Kobayashi, H., H. Ohi, H. Shinohara, M. Sugimura, T. Fujii, T. Terao, M. Schmitt, L. Goretzki, N. Chucholowski, and F. Janicke. 1993. Saturation of tumour cell surface receptors for urokinase-type plasminogen activator by amino-terminal fragment and subsequent effect on reconstituted basement membranes invasion. Br. J. Cancer 67:537-544.
34. Krasnykh, V., I. Dmitriev, G. Mikheeva, C. R. Miller, N. Belousova, and D. T. Curiel. 1998. Characterization of an adenovirus vector containing a heterologous peptide epitope in the HI loop of the fiber knob. J. Virol. 72:1844-1852.
35. Landgraf, R., M. Pegram, D. J. Slamon, and D. Eisenberg. 1998. Cytotoxicity and specificity of directed toxins composed of diphtheria toxin and the EGF-like domain of heregulin betal. Biochemistry 37:3220-3228.
36. Liddington, R. C., Y. Yan, J. Moulai, R. Sahli, T. L. Benjamin, and S. C. Harrison. 1991. Structure of simian virus 40 at 3.8-A resolution. Nature 354:278-284.
37. Liu, W. J., X. S. Liu, K. N. Zhao, G. R. Leggatt, and I. H. Frazer. 2000. Papillomavirus virus-like particles for the delivery of multiple cytotoxic T cell epitopes. Virology 273:374-382.
38. Magnusson, M. K., S. S. Hong, P. Henning, P. Boulanger, and L. Lindholm. 2002. Genetic retargeting of adenovirus vectors: functionality of targeting ligands and their influence on virus viability. J. Gene Med. 4:356-370.
39. Mezes, B., and P. Amati. 1994. Mutations of polyomavirus VP1 allow in vitro growth in undifferentiated cells and modify in vivo tissue replication specificity. J. Virol. 68:1196-1199.
40. Miyazaki, M., N. Lamharzi, A. V. Schally, G. Halmos, K. Szepeshazi, K. Groot, and R. Z. Cai. 1998. Inhibition of growth of MDA-MB-231 human breast cancer xenografts in nude mice by bombesin/gastrin-releasing peptide (GRP) antagonists RC-3940-II and RC-3095. Eur. J. Cancer 34:710-717.
41. Muller, M., J. Zhou, T. D. Reed, C. Rittmuller, A. Burger, J. Gabelsberger, J. Braspenning, and L. Gissmann. 1997. Chimeric papillomavirus-like particles. Virology 234:93-111.
42. Nusrat, A. R., and H. A. Chapman, Jr. 1991. An autocrine role for urokinase in phorbol ester-mediated differentiation of myeloid cell lines. J. Clin. Investig. 87:1091-1097.
43. Ossowski, L. 1988. In vivo invasion of modified chorioallantoic membrane by tumor cells: the role of cell surface-bound urokinase. J. Cell Biol. 107:2437-2445.
44. Pansky, A., F. Peng, M. Eberhard, L. Baselgia, W. Siegrist, J. B. Baumann, A. N. Eberle, C. Beglinger, and P. Hildebrand. 1997. Identification of functional GRP-preferring bombesin receptors on human melanoma cells. Eur. J. Clin. Investig. 27:69-76.
45. Peng, S., I. H. Frazer, G. J. Fernando, and J. Zhou. 1998. Papillomavirus virus-like particles can deliver defined CTL epitopes to the MHC class I pathway. Virology 240:147-157.
46. Pepper, M. S., A. P. Sappino, R. Stocklin, R. Montesano, L. Orci, and J. D. Vassalli. 1993. Upregulation of urokinase receptor expression on migrating endothelial cells. J. Cell Biol. 122:673-684.
47. Picone, R., E. L. Kajtaniak, L. S. Nielsen, N. Behrendt, M. R. Mastronicola, M. V. Cubellis, M. P. Stoppelli, S. Pedersen, K. Dano, and F. Blasi. 1989. Regulation of urokinase receptors in monocytelike U937 cells by phorbol ester phorbol myristate acetate. J. Cell Biol. 108:693-702.
48. Plesner, T., M. Ploug, V. Ellis, E. Ronne, G. Hoyer-Hansen, M. Wittrup, T. L. Pedersen, T. Tscherning, K. Dano, and N. E. Hansen. 1994. The receptor for urokinase-type plasminogen activator and urokinase is translocated from two distinct intracellular compartments to the plasma membrane on stimulation of human neutrophils. Blood 83:808-815.
49. Plowman, G. D., J. M. Culouscou, G. S. Whitney, J. M. Green, G. W. Carlton, L. Foy, M. G. Neubauer, and M. Shoyab. 1993. Ligand-specific activation of HER4/p180erbB4, a fourth member of the epidermal growth factor receptor family. Proc. Natl. Acad. Sci. USA 90:1746-1750.
50. Rajagopal, V., and R. J. Kreitman. 2000. Recombinant toxins that bind to the urokinase receptor are cytotoxic without requiring binding to the alpha(2)-macroglobulin receptor. J. Biol. Chem. 275:7566-7573.
51. Rayment, I., T. S. Baker, D. L. Caspar, and W. T. Murakami. 1982. Polyoma virus capsid structure at 22.5 A resolution. Nature 295:110-115.
52. Resnati, M., M. Guttinger, S. Valcamonica, N. Sidenius, F. Blasi, and F. Fazioli. 1996. Proteolytic cleavage of the urokinase receptor substitutes for the agonist-induced chemotactic effect. EMBO J. 15:1572-1582.
53. Ricci, L., R. Maione, C. Passananti, A. Felsani, and P. Amati. 1992. Mutations in the VP1 coding region of polyomavirus determine differentiating stage specificity. J. Virol. 66:7153-7158.
54. Richterova, Z., D. Liebl, M. Horak, Z. Palkova, J. Stokrova, P. Hozak, J. Korb, and J. Forstova. 2001. Caveolae are involved in the trafficking of mouse polyomavirus virions and artificial VP1 pseudocapsids toward cell nuclei. J. Virol. 75:10880-10891.
55. Salunke, D. M., D. L. Caspar, and R. L. Garcea. 1986. Self-assembly of purified polyomavirus capsid protein VP1. Cell. 46:895-904.
56. Salunke, D. M., D. L. Caspar, and R. L. Garcea. 1989. Polymorphism in the assembly of polyomavirus capsid protein VP1. Biophys. J. 56:887-900.
57. Schmidt, U., R. Rudolph, and G. Bohm. 2001. Binding of external ligands onto an engineered virus capsid. Protein Eng. 14:769-774.
58. Stehle, T., and S. C. Harrison. 1996. Crystal structures of murine polyomavirus in complex with straight-chain and branched-chain sialyloligosaccharide receptor fragments. Structure 4:183-194.
59. Stehle, T., and S. C. Harrison. 1997. High-resolution structure of a polyomavirus VP1-oligosaccharide complex: implications for assembly and receptor binding. EMBO J. 16:5139-5148.
60. Stehle, T., Y. Yan, T. L. Benjamin, and S. C. Harrison. 1994. Structure of murine polyomavirus complexed with an oligosaccharide receptor fragment. Nature 369:160-163.
61. Stoppelli, M. P., A. Corti, A. Soffientini, G. Cassani, F. Blasi, and R. K. Assoian. 1985. Differentiation-enhanced binding of the amino-terminal fragment of human urokinase plasminogen activator to a specific receptor on U937 monocytes. Proc. Natl. Acad. Sci. USA 82:4939-4943.
62. Stubenrauch, K., S. Gleiter, U. Brinkmann, R. Rudolph, and H. Lilie. 2001. Conjugation of an antibody Fv fragment to a virus coat protein: cell-specific targeting of recombinant polyoma-virus-like particles. Biochem. J. 356:867-873.
63. Testa, J. E., and J. P. Quigley. 1990. The role of urokinase-type plasminogen activator in aggressive tumor cell behavior. Cancer Metastasis Rev. 9:353-367.
64. Thorne, H. V., W. House, and A. L. Kisch. 1965. Electrophoretic properties and purification of large and small plaque-forming strains of polyoma virus. Virology 27:37-43.
65. Tindle, R. W., K. Herd, P. Londono, G. J. Fernando, S. N. Chatfield, K. Malcolm, and G. Dougan. 1994. Chimeric hepatitis B core antigen particles containing B- and Th-epitopes of human papillomavirus type 16 E7 protein induce specific antibody and T-helper responses in immunised mice. Virology 200:547-557.
66. Wei, Y., D. A. Waltz, N. Rao, R. J. Drummond, S. Rosenberg, and H. A. Chapman. 1994. Identification of the urokinase receptor as an adhesion receptor for vitronectin. J. Biol. Chem. 269:32380-32388.
67. Yano, T., J. Pinski, K. Groot, and A. V. Schally. 1992. Stimulation by bombesin and inhibition by bombesin/gastrin-releasing peptide antagonist RC-3095 of growth of human breast cancer cell lines. Cancer Res. 52:4545-4547.